Skip to main content
Log in

Early development of descending pathways from the brain stem to the spinal cord in Xenopus laevis

  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

The early development of descending pathways from the brain stem to the spinal cord has been studied in Xenopus laevis tadpoles. The relatively protracted development of this permanently aquatic amphibian as well as its transparency during development make this animal particularly attractive for experimental studies. Between the 5th and 10th myotome the spinal cord was crushed with a thin needle and dry horseradish peroxidase (HRP) crystals were applied. After a survival time of one day the tadpoles were fixed and the brain and spinal cord were stained as a whole according to a modification of the heavy metal intensification of the DAB-reaction, cleared in cedarwood oil and examined as wholemounts.

At stage 28 (the neural tube has just closed) the first brain stem neurons projecting to the spinal cord were found in what appear to be the nucleus reticularis inferior and medius. At this stage of development the first, uncoordinated swimming movements can be observed. At stage 30/31 (the tailbud is visible) both Mauthner cells project to the spinal cord as well as the interstitial nucleus of the fasciculus longitudinalis medialis situated in the mesencephalon. Towards stage 35/36 (the tail is now clearly visible), a more extensive reticulospinal innervation of the spinal cord appears, now including cells of the nucleus reticularis superior. At this stage also the first vestibulospinal and raphespinal projections were found. At stage 43/44 (the tadpoles have now a well-developed tail) the pattern of reticulospinal projections appears to be completed with the presence of labeled neutrons in the nucleus reticularis isthmi. From stage 43/44 on, the number of HRP-positive cells is steadily increasing. At stage 47/48, when the hindlimb buds appear, the descending projections to the spinal cord are comparable with the adult situation except for the absence of a rubrospinal and a hypothalamospinal projection.

The observations demonstrate that already very early in development reticulospinal fibers and, somewhat later, Mauthner cell axons and vestibulospinal fibers innervate the spinal cord. Furthermore, a caudorostral gradient appears to exist with regard to the development of descending projections to the spinal cord. However, the interstitial nucleus of the fasciculus longitudinalis medialis forms an exception to this rule.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adams JC (1981) Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem 29:775

    Google Scholar 

  • Altman JS, Bayer SA (1980a) Development of the brain stem in the rat. I: Thymidine-radiographic study of the time of origin of neurons of the lower medulla. J Comp Neurol 194:1–35

    Google Scholar 

  • Altman JS, Bayer SA (1980b) Development of the brain stem in the rat. II: Thymidine-radiographic study of the time of origin of neurons of the upper medulla, excluding the vestibular and auditory nuclei. J Comp Neurol 194:37–56

    Google Scholar 

  • Altman JS, Bayer SA (1980c) Development of the brain stem in the rat. III: Thymidine-radiographic study of the time of origin of neurons of the vestibular and auditory nuclei of the upper medulla. J Comp Neurol 194:877–904

    Google Scholar 

  • Billings SM (1972) Development of the Mauthner cell in Xenopus laevis: a light and electron microscopic study of the perikaryon. Z Anat Entiwicklungsgesch 136:168–191

    Google Scholar 

  • Blight AR (1976) Undulatory swimming with and without waves of contraction. Nature (Lond.) 264:352–354

    Google Scholar 

  • Blight AR (1977) The muscular control of vertebrate swimming movements. Biol Rev 52:181–218

    Google Scholar 

  • Cabana T, Martin GF (1982) The origin of brain stem-spinal projections at different stages of development in the North American opossum. Dev Brain Res 2:163–168

    Google Scholar 

  • Coghill GE (1913) The primary ventral roots and somatic motor collumn of Amblystoma. J Comp Neurol 23:21–143

    Google Scholar 

  • Coghill GE (1914) Correlated anatomical and physiological studies of the growth of the nervous system of amphibia I: the afferent system of the trunk of Amblystoma. J Comp Neurol 24:161–233

    Google Scholar 

  • Coghill GE (1929) Anatomy and the problem of behaviour. Cambridge University Press, Cambridge

    Google Scholar 

  • DiTirro FJ, Martin GF, Ho RH (1983) A developmental study of substance P, somatostatin, enkephalin, and serotonin immunoreactive elements in the spinal cord of the North American opossum. J Comp Neurol 213:241–261

    Google Scholar 

  • Dubé L, Parent A (1982) The organization of monoamine-containing neurons in the brain of the salamander Necturus maculosus. J Comp Neurol 211:21–30

    Google Scholar 

  • Forehand CJ, Farel PB (1982) Spinal cord development in anuran larvae: II. Ascending and descending pathways. J Comp Neurol 209:395–408

    Google Scholar 

  • Gonzalez A, ten Donkelaar HJ, de Boer-van Huizen R (1984) Cerebellar connections in Xenopus laevis: an HRP study. Anat Embryol 169:167–176

    Google Scholar 

  • Grillner S (1981) Control of locomotion in bipeds, tetrapeds, and fish. In: Brooks VB (ed) Handbook of Physiology, Sect 1 Vol 2: Motor control. American Physiol Soc Bethesda, pp 1179–1236

    Google Scholar 

  • Humbertson AO, Martin GF (1979) The development of monoaminergic brain stem-spinal systems in the North American opossum. Anat Embryol 156:301–318

    Google Scholar 

  • Jacobson M (1978) Developmental neurobiology. Plenum Press, New York London

    Google Scholar 

  • Jacoby J, Rubinson K (1983) The acoustic and lateral line nuclei are distinct in the premetamorphic frog, Rana catesbeiana. J Comp Neurol 216:152–161

    Google Scholar 

  • Kahn JA, Roberts A (1982a) Experiments on the central pattern generator for swimming in amphibian embryos. Phil Trans R Soc London B 296:229–243

    Google Scholar 

  • Kahn JA, Roberts A (1982b) The central nervous origin of the swimming motor pattern in embryos of Xenopus laevis. J Exp Biol 99:185–196

    Google Scholar 

  • Kahn JA, Roberts A, Kashin SM (1982) The neuromuscular basis of swimming movements in embryos of the amphibian Xenopus laevis. J Exp Biol 99:175–184

    Google Scholar 

  • Kevetter GA, Lasek RJ (1982) Development of the marginal zone in the rhombencephalon of Xenopus laevis. Dev Brain Res 4:195–208

    Google Scholar 

  • Kimmel CB (1982) Reticulospinal and vestibulospinal neurons in the young larva of a teleost fish, Brachidanio rerio. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord. Progress in Brain Research, vol 57. Elsevier Biomedical Press, Amsterdam New York Oxford, pp 1–24

    Google Scholar 

  • Kimmel CB, Model PG (1978) Developmental studies of the Mauthner cell. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 183–220

    Google Scholar 

  • Kimmel CB, Powell SL, Metcalfe WR (1982) Brain neurons which project to the spinal cord in young larvae of the zebrafish. J Comp Neurol 205:112–127

    Google Scholar 

  • Kuypers HGJM, Martin GF (1982) Descending pathways to the spinal cord. Progress in Brain Research, vol 57. Elsevier Biomedical Press, Amsterdam New York Oxford

    Google Scholar 

  • Lamborghini JE (1980) Rohon-Beard cells and other large neurons in Xenopus embryos originate during gastrulation. J Comp Neurol 189:323–333

    Google Scholar 

  • Lidov HGW, Molliver ME (1982) Immunohistochemical study of the development of serotonergic neurons in the rat CNS. Brain Res Bull 9:559–604

    Google Scholar 

  • Martin GF, Beals JK, Culberson JL, Dom R, Goode G, Humbertson AO (1978) Observations on the development of brain stemspinal systems in the North American opossum. J Comp Neurol 181:271–290

    Google Scholar 

  • Martin GF, Cabane T, DiTirro FJ, Ho RH, Humbertson AO (1982) The development of descending spinal connections. Studies using the North American opossum. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord. Progress in Brain Research, vol 57. Elsevier Biomedical Press, Amsterdam New York Oxford, pp 131–144

    Google Scholar 

  • Mesulam MM (1978) Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reactionproduct with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    Google Scholar 

  • Mesulam MM (1982) Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways — axonal transport, enzyme histochemistry and lightmicroscopic analysis. In: Mesulam MM (ed) Tracing neural connections with horseradish peroxidase. IBRO Handbook Series Methods in the Neurosciences, vol 1. John Wiley and Sons, Chichester, pp 1–152

    Google Scholar 

  • Muntz L (1964) Neuromuscular foundation of behaviour in embryonic and larval stages of the anuran, Xenopus laevis. Ph D Thesis, Bristol University, Bristol

  • Nieuwenhuys R (1977) The brain of the lamprey in a comparative perspective. Ann New York Acad Sci 229:97–145

    Google Scholar 

  • Nieuwkoop PD, Faber J (1967) Normal table of Xenopus laevis (Daudin). North Holland Publ Co Amsterdam

    Google Scholar 

  • Nukundiwe AM, Nieuwenhuys R (1983) The cell masses in the brain stem of the South African clawed frog Xenopus laevis: a topographical and topological analysis. J Comp Neurol 213:199–219

    Google Scholar 

  • Nordlander RH, Ryba TJ (1983) Development of supraspinal input into the tail spinal cord of Xenopus. Soc Neurosci Abstr 9:847

    Google Scholar 

  • Nornes HO, Morita M (1979) Time of origin of the neurons in the caudal brain stem of rat: an autoradiographic study. Dev Neurosci 2:101–114

    Google Scholar 

  • Rager G, Lausmann S, Gallyas F (1979) An improved silverstain for developing nervous tissue. Stain Technol 54:193–200

    Google Scholar 

  • Roberts A (1971) The role of propagated skin impulses in the sensory system of young tadpoles. Z Vergl Physiol 75:388–401

    Google Scholar 

  • Roberts A, Clarke JDW (1982) The neuroanatomy of an amphibian embryo spinal cord. Phil Trans R Soc London B 296:195–212

    Google Scholar 

  • Roberts A, Kahn JA, Soffe SR, Clarke JDW (1981) Neural control of swimming in a vertebrate. Science 213:1032–1034

    Google Scholar 

  • Rovainen CM (1978) Müller cells, Mauthner cells, and other identified reticulospinal neurons in the lamprey. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 245–269

    Google Scholar 

  • Rovainen CM (1979) Neurobiology of lampreys. Physiol Rev 59:1007–1077

    Google Scholar 

  • Sims TJ (1977) The development of monoamine-containing neurons in the brain and spinal cord of the salamander, Ambystoma mexicanum. J Comp Neurol 173:319–336

    Google Scholar 

  • Stchouwer AJ, Farel PB (1980) Central and peripheral controls of swimming in anuran larvae. Brain Res 195:323–335

    Google Scholar 

  • Stchouwer AJ, Farel PB (1983) Development of hindlimb locomotor activity in the bullforg studied in vitro. Science 219:516–518

    Google Scholar 

  • Steinbusch HWM, Verhofstad AAJ, Joosten HWJ (1983) Antibodies to serotonin for neuroimmunocytochemical studies on the central nervous system. In: Cuello C (ed) Neuroimmunocytochemistry. IBRO Handbook Series Methods in the Neurosciences, vol 3. John Wiley and Sons, Chichester, pp 193–214

    Google Scholar 

  • Taber-Pierce E (1973) Time of origin of neurons in the brain stem of the mouse. Progr Brain Res 40:53–65

    Google Scholar 

  • Taylor AC, Kollros JJ (1946) Stages in normal development of Rana pipiens larvae. Anat Rec 94:7–23

    Google Scholar 

  • Ten Donkelaar HJ (1982) Organization of descending pathways to the spinal cord in amphibians and reptiles. In: Kuypers HGJM, Martin GF (eds) Descending pathways to the spinal cord. Progress in Brain Research, vol 57. Elsevier Biomedical Press, Amsterdam, pp 131–144

    Google Scholar 

  • Ten Donkelaar HJ, de Boer-van Huizen R (1982) Observations on the development of descending pathways from the brain stem to the spinal cord in the clawed toad Xenopus laevis. Anat Embryol 163:461–473

    Google Scholar 

  • Ten Donkelaar HJ, de Boer-van Huizen R, Schouten FTM, Eggen SJH (1981) Cells of origin of descending pathways to the spinal cord in the clawed toad (Xenopus laevis). Neuroscience 6:2297–2312

    Google Scholar 

  • Ten Donkelaar HJ, Kusuma A, de Boer-van Huizen R (1980) Cells of origin of descending pathways to the spinal cord in some quadrupedal reptiles. J Comp Neurol 192:827–851

    Google Scholar 

  • Ueda S, Nojyo Y, Sano Y (1984) Immunohistochemical demonstration of the serotonin neuron system in the central nervous system of the bullfrog, Rana catesbeiana. Anat Embryol 169:219–229

    Google Scholar 

  • Vargas-Lizardi P, Lyser KM (1974) Time of origin of Mauthner's neuron in Xenopus laevis embryos. Dev Biol 38:220–228

    Google Scholar 

  • Wallace JA, Lauder JM (1983) Development of the serotonergic system in the rat embryo: an immunocytochemical study. Brain Res Bull 10:459–479

    Google Scholar 

  • Whiting HP (1957) Mauthner neurons in young larval lampreys. Q J Micros 98:163–178

    Google Scholar 

  • Zottoli SJ (1978) Comparative morphology of the Mauthner cell in fish and amphibians. In: Faber DS, Korn H (eds) Neurobiology of the Mauthner cell. Raven Press, New York, pp 13–46

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

van Mier, P., ten Donkelaar, H.J. Early development of descending pathways from the brain stem to the spinal cord in Xenopus laevis . Anat Embryol 170, 295–306 (1984). https://doi.org/10.1007/BF00318733

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318733

Key words

Navigation